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This page intentionally left blank
Introductory Biomechanics
From Cells to Organisms

Introductory Biomechanics is a new, integrated text written specifically for

engineering students. It provides a broad overview of this important branch of the
rapidly growing field of bioengineering. A wide selection of topics is presented,
ranging from the mechanics of single cells to the dynamics of human movement.
No prior biological knowledge is assumed and in each chapter, the relevant
anatomy and physiology are first described. The biological system is then
analyzed from a mechanical viewpoint by reducing it to its essential elements,
using the laws of mechanics, and then linking mechanical insights back to
biological function. This integrated approach provides students with a deeper
understanding of both the mechanics and the biology than that obtained from
qualitative study alone. The text is supported by a wealth of illustrations, tables,
and examples, a large selection of suitable problems and many current references,
making it an essential textbook for any biomechanics course.

C. Ross Ethier is a Professor of Mechanical and Industrial Engineering, the

Canada Research Chair in Computational Mechanics, and the Director of the
Institute of Biomaterials and Biomedical Engineering at the University of Toronto,
with cross-appointment to the Department of Ophthalmology and Vision Sciences.
His research focuses on biomechanical factors in glaucoma and on blood flow and
mass transfer in the large arteries. He has taught biomechanics for over 10 years.

Craig A. Simmons is the Canada Research Chair in Mechanobiology and an

Assistant Professor in the Department of Mechanical and Industrial Engineering at
the University of Toronto, with cross-appointments to the Institute of Biomaterials
and Biomedical Engineering and the Faculty of Dentistry. His research interests
include cell and tissue biomechanics and cell mechanobiology, particularly as it
relates to tissue engineering and heart valve disease.
Cambridge Texts in Biomedical Engineering

Series Editors
Professor Mark Saltzman Yale University
Professor Shu Chien University of California, San Diego
Professor William Hendee Medical College of Wisconsin
Professor Roger Kamm Massachusetts Institute of Technology
Professor Robert Malkin Duke University
Professor Alison Noble Oxford University

Cambridge Texts in Biomedical Engineering provides a forum for high-quality,

accessible textbooks targeted at undergraduate and graduate courses in biomedical
engineering. It will cover a broad range of biomedical engineering topics from
introductory texts to advanced topics including, but not limited to, biomechanics,
physiology, biomedical instrumentation, imaging, signals and systems, cell
engineering, and bioinformatics. The series will blend theory and practice, aimed
primarily at biomedical engineering students but will be suitable for broader
courses in engineering, the life sciences and medicine.
Introductory Biomechanics
From Cells to Organisms

C. Ross Ethier and Craig A. Simmons

University of Toronto, Canada
CAMBRIDGE UNIVERSITY PRESS
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo

Cambridge University Press

The Edinburgh Building, Cambridge CB2 8RU, UK
Published in the United States of America by Cambridge University Press, New York
www.cambridge.org
Information on this title: www.cambridge.org/9780521841122

© C. R. Ethier and C. A. Simmons 2007

This publication is in copyright. Subject to statutory exception and to the provision of

relevant collective licensing agreements, no reproduction of any part may take place
without the written permission of Cambridge University Press.

First published in print format 2007

ISBN-13 978-0-511-27360-5 eBook (EBL)

ISBN-10 0-511-27360-6 eBook (EBL)

ISBN-13 978-0-521-84112-2 hardback

ISBN-10 0-521-84112-7 hardback

Cambridge University Press has no responsibility for the persistence or accuracy of urls
for external or third-party internet websites referred to in this publication, and does not
guarantee that any content on such websites is, or will remain, accurate or appropriate.
To my family, who make it all worthwhile.
c. ross eth i er

To Deborah,
and to my parents, who inspired my love of learning.
craig a. simmons
Contents

About the cover page xii

Preface xv

1 Introduction 1
1.1 A brief history of biomechanics 3
1.2 An outline of this book 12
References 15

2 Cellular biomechanics 18
2.1 Introduction to eukaryotic cellular architecture 18
2.2 The cell’s energy system 22
2.3 Overview of the cytoskeleton 23
2.3.1 Actin filaments 25
2.3.2 Intermediate filaments 28
2.3.3 Microtubules 28
2.4 Cell–matrix interactions 29
2.5 Methods to measure the mechanical properties of cells
and biomolecules 35
2.5.1 Atomic force microscopy 35
2.5.2 Optical trapping (“optical tweezers”) 41
2.5.3 Magnetic bead microrheometry 42
2.5.4 Micropipette aspiration 43
2.6 Models of cellular biomechanical behavior 53
2.6.1 Lumped parameter viscoelastic model of the cell 54
2.6.2 Tensegrity model of the cytoskeleton 60
2.6.3 Modeling actin filaments as a foam 69
2.6.4 Computational model of a chondrocyte in its matrix 72
2.7 Mechanotransduction: how do cells sense and respond to
mechanical events? 76
2.7.1 Mechanoreceptors 76
2.7.2 Intracellular signal transduction 78
2.7.3 Cellular response to mechanical signals 80
viii Contents

2.8 Techniques for mechanical stimulation of cells 80

2.8.1 Compressive loading 81
2.8.2 Stretching 82
2.8.3 Fluid flow 86
2.9 Summary of mechanobiological effects on cells in
selected tissues 90
2.9.1 Endothelial cells in the vascular system 91
2.9.2 Smooth muscle cells in vascular tissue 93
2.9.3 Chondrocytes in articular cartilage 94
2.9.4 Osteoblasts and osteocytes in bone 95
2.10 Problems 99
References 111

3 Hemodynamics 119
3.1 Blood rheology 119
3.1.1 Blood composition 121
3.1.2 Relationship between blood composition and rheology 124
3.1.3 Constitutive equation for blood 129
3.2 Large artery hemodynamics 130
3.2.1 Physical characteristics of blood flow patterns in vivo 130
3.2.2 Steady blood flow at low flow rates 133
3.2.3 Unsteady flow in large vessels 138
3.3 Blood flow in small vessels 142
3.3.1 Fahraeus–Lindqvist effect 143
3.3.2 “Inverse” Fahraeus–Lindqvist effect 146
3.4 Problems 147
References 161

4 The circulatory system 164

4.1 Anatomy of the vasculature 164
4.2 The heart 169
4.2.1 Gross anatomy of the heart 171
4.2.2 Qualitative description of cardiac pumping 172
4.2.3 Cardiac pumping power and ventricular function 175
4.3 Arterial pulse propagation 179
4.3.1 Systolic and diastolic pressure 179
4.3.2 Windkessel model 180
4.3.3 Arterial wall structure and elasticity 183
4.3.4 Elastic waves 186
4.3.5 Pressure–flow relationships: purely oscillatory flow 194
ix Contents

4.3.6 Pressure–flow relationships: mean flow effects 197

4.3.7 Pressure–flow relationships: deviations from ideality 198
4.4 The capillaries 204
4.4.1 Capillary filtration: the experiments of Landis 207
4.4.2 Osmotic pressure 209
4.4.3 Quantitative analysis of capillary leakage 211
4.5 The veins 212
4.6 Scaling of hemodynamic variables 213
4.7 Problems 218
References 235

5 The interstitium 240

5.1 Interstitial fluid flow 240
5.1.1 Darcy’s law 241
5.1.2 Clearance of edema 242
5.2 Problems 248
References 249

6 Ocular biomechanics 250

6.1 Ocular anatomy 250
6.2 Biomechanics of glaucoma 251
6.2.1 Tonometry 252
6.2.2 Drainage of aqueous humor in normal and glaucomatous eyes 257
6.2.3 Aqueous humor circulation in the anterior chamber 263
6.2.4 Optic nerve head biomechanics 264
6.3 Ocular blood flow 271
6.4 Problems 274
References 276

7 The respiratory system 282

7.1 Gross anatomy 282
7.1.1 The conducting airways and pulmonary vasculature 282
7.1.2 Associated structures 285
7.2 Biomechanics of breathing 287
7.3 Lung elasticity and surface tension effects 288
7.4 Mass transfer 294
7.4.1 Blood-side acinar mass transfer 295
7.4.2 Air-side acinar mass transfer 307
7.4.3 Whole lung mass transfer 308
7.5 Particle transport in the lung 313
x Contents

7.6 Problems 316

References 329

8 Muscles and movement 332

8.1 Skeletal muscle morphology and physiology 333
8.1.1 Isotonic versus isometric contraction 339
8.2 Muscle constitutive modeling 343
8.3 Whole muscle mechanics 351
8.3.1 Parallel versus pinnate muscle types 351
8.4 Muscle/bone interactions 353
8.4.1 Foreleg motion in two species 353
8.4.2 Flexion of the elbow 355
8.4.3 Biomechanics of the knee 365
8.5 Problems 369
References 376

9 Skeletal biomechanics 379

9.1 Introduction to bone 379
9.2 Composition and structure of bone 382
9.2.1 Cortical bone 384
9.2.2 Trabecular bone 384
9.3 Biomechanical properties of cortical and trabecular bone 387
9.3.1 Cortical bone mechanics 388
9.3.2 Trabecular bone mechanics 389
9.3.3 Trabecular bone mechanics: density dependence 390
9.3.4 Trabecular bone mechanics: unit cell models 393
9.4 Bone fracture and failure mechanics 395
9.4.1 Fast fracture 397
9.4.2 Fatigue fracture 403
9.5 Functional adaptation and mechanobiology 407
9.6 The design of bone 409
9.7 Introduction to soft connective tissues 411
9.8 Structure of collagen 412
9.9 Structure of ligament, tendon, and cartilage 414
9.9.1 Ligament 414
9.9.2 Tendon 416
9.9.3 Cartilage 418
9.10 Biomechanical properties of ligament, tendon, and cartilage 419
9.10.1 Structural properties 420
9.10.2 Material properties 423
9.10.3 Material properties: tension 425
xi Contents

9.10.4 Material properties: compression 426

9.10.5 Material properties: viscoelasticity 428
9.10.6 Material properties: biphasic mixture theory of cartilage 435
9.11 Problems 436
References 439

10 Terrestrial locomotion 444

10.1 Jumping 444
10.1.1 Standing jump 444
10.1.2 Running jumps 448
10.2 Description of walking and running 451
10.2.1 Walking 451
10.2.2 Running 459
10.3 Gait analysis 461
10.3.1 Kinematics 463
10.3.2 Anthropometry 468
10.3.3 Kinetics 471
10.4 Problems 480
References 487

Appendix The electrocardiogram 489

Index 498

Color plate section between pages 118 and 119

About the cover

The cover contains images that together represent the broad scope of modern
biomechanics. The figures are as follows:
r Main image: A fluorescent immunohistochemical image of an endothelial cell
isolated from the surface of a pig aortic heart valve and grown in culture. Within
the cell, the nucleus is stained blue and vimentin filaments are stained green.
Vimentin is an intermediate filament protein of the cellular cytoskeleton that
plays an important role in cellular mechanics.
r Left top: An intermediate stage from a simulation of the forced unfolding of
repeats 4 and 5 of chain A of the protein filamin. Filamin is an actin cross-linking
protein and therefore plays a role in the biomechanics of the cytoskeleton. The
simulation was based on the crystal structure of part of filamin [1], and was
carried out in NAMD [2] and visualized using the VMD package [3]. (Image
courtesy of Mr. Blake Charlebois.)
r Left middle: A sketch by the Swiss anatomist Hermann von Meyer of the
orientation of trabecular bone in the proximal human femur. This sketch was
accompanied in the original article by a sketch of the principal stress trajectories
in a crane having a shape similar to the femur. Together these sketches are
believed to have inspired “Wolff’s Law” of bone remodelling. From [4].
r Left lower: The distribution of mass transfer rates from flowing blood to cultured
vascular endothelial cells. The contoured quantity (the Sherwood number) was
computed by first measuring the topography of the endothelial cells using atomic
force microscopy and then solving the convection-diffusion equation in the
blood flowing over the cells. Mass transfer from blood to endothelial cells is
important in cell-cell signalling. (Image courtesy of Mr. Ji Zhang.)

References

1. G. M. Popowicz, R. Muller, A. A. Noegel, M. Schleicher, R. Huber and T. A. Holak.

Molecular structure of the rod domain of dictyostelium filamin. Journal of Molecular
Biology, 342 (2004), 1637–1646.
xiii About the cover

2. L. Kale, R. Skeel, M. Bhandarkar, R. Brunner, A. Gursoy, N. Krawetz et al. NAMD2:

Greater scalability for parallel molecular dynamics. Journal of Computational Physics,
151 (1999), 283–312.
3. W. Humphrey, A. Dalke and K. Schulten. VMD: Visual Molecular Dynamics. Journal
of Molecular Graphics, 14 (1996), 33–38.
4. J. Wolff. Über die innere Architectur der Knochen und ihre Bedeutung für die Frage
vom Knochenwachsthum. Archiv für Pathologische Anatomie und Physiologie und für
Klinische Medicin, 50 (1870), 389–450.
Preface

For some years, we have taught an introductory course in biomechanics within

the Department of Mechanical and Industrial Engineering at the University of
Toronto. We have been unable to find a textbook suitable for the purpose of intro-
ducing engineers and others having a “hard science” background to the field of
biomechanics. That is not to say that excellent books on biomechanics do not exist;
in fact, there are many. However, they are typically at a level that is too advanced
for an introductory course, or they cover too limited a subset of topics for purposes
of an introductory course.
This book represents an attempt to fill this void. It is not meant to be an extensive
treatise on any particular branch of biomechanics, but rather to be an introduction
to a wide selection of biomechanics-related topics. Our hope is that it will aid the
student in his or her introduction to the fascinating world of bioengineering, and
will lead some to pursue the topic in greater detail.
In writing this book, we have assumed that the reader has a background in
engineering and mathematics, which includes introductory courses in dynamics,
statics, fluid mechanics, thermodynamics, and solid mechanics. No prior knowl-
edge of biology, anatomy, or physiology is assumed, and in fact every section begins
with a review of the relevant biological background. Each chapter then emphasizes
identification and description of the essential aspects of the related biomechanics
problems. Because of the introductory nature of this book, this has led in some
cases to a great deal of simplification, but in all instances, we have tried to maintain
a firm link to “biological reality.”
We wish to thank Professor David F. James, of the Department of Mechanical
and Industrial Engineering, University of Toronto. He first developed the introduc-
tory course in biomechanical engineering at the University and his course notes
provided the inspiration for parts of this book. Professors James E. Moore Jr.
and Takami Yamaguchi provided important material for Ch. 1. We have benefited
greatly from interactions with our students, who sometimes are the best teachers,
and our colleagues and mentors.
We shall be most grateful to students who, upon discovering errors in the text,
bring them to our attention.
1 Introduction

Biomechanics is a branch of the field of bioengineering, which we define as the

application of engineering principles to biological systems. Most bioengineering
is applied to humans, and in this book the primary emphasis will be on Homo
sapiens. The bioengineer seeks to understand basic physiological processes, to
improve human health via applied problem solving, or both. This is a difficult task,
since the workings of the body are formidably complex. Despite this difficulty,
the bioengineer’s contribution can be substantial, and the rewards for success far
outweigh the difficulties of the task.
Biomechanics is the study of how physical forces interact with living systems. If
you are not familiar with biomechanics, this might strike you as a somewhat esoteric
topic, and you may even ask yourself the question: Why does biomechanics matter?
It turns out that biomechanics is far from esoteric and plays an important role in
diverse areas of growth, development, tissue remodeling and homeostasis. Further,
biomechanics plays a central role in the pathogenesis of some diseases, and in the
treatment of these diseases. Let us give a few specific examples:

r How do your bones “know” how big and strong to be so that they can support
your weight and deal with the loads imposed on them? Evidence shows that
the growth of bone is driven by mechanical stimuli [1]. More specifically,
mechanical stresses and strains induce bone cells (osteoblasts and osteoclasts)
to add or remove bone just where it is needed. Because of the obvious mechanical
function played by bone, it makes good sense to use mechanical stress as the
feedback signal for bone growth and remodeling. But biomechanics also plays
a “hidden” regulatory role in other growth processes, as the next example will
show.
r How do our arteries “know” how big to be so that they can deliver just the right
amount of blood to their distal capillary beds? There is good evidence that this
is determined in large part by the mechanical stress exerted on the artery wall by
flowing blood. Endothelial cells lining the inner arterial surface sense this shear
stress and send signals to cells deeper in the artery wall to direct the remodeling
of the artery so as to enlarge or reduce its caliber [2].
2 Introduction

r What about biomechanics in everyday life? Probably the most obvious appli-
cation of biomechanics is in locomotion (walking, running, jumping), where
our muscles generate forces that are transferred to the ground by bones and soft
connective tissue. This is so commonplace that we rarely think about it, yet the
biomechanics of locomotion is remarkably complex (watch a baby learning to
walk!) and still incompletely understood.
r Locomotion happens on many scales, from whole organisms all the way down
to individual cells. Unicellular organisms must be able to move so as to gather
nutrients, and they have evolved a variety of clever strategies to accomplish
this task [3]. In multicellular organisms, the ability of single cells to move is
essential in processes such as repair of wounds, capture of foreign pathogens,
and tissue differentiation. Force generation at the cellular level is a fascinating
topic that is the subject of much active research.
r Cells can generate forces, but just as importantly, they can sense and respond
to forces. We alluded to this above in the examples of bone remodeling and
arterial caliber adjustment, but it is not only endothelial and bone cells that
can sense forces. In fact, the ability of mechanical stress to elicit a biological
response in cells seems to be the rule rather than the exception, and some cells
are exquisitely specialized for just this task. One remarkable example is the
hair cells in the ear. These cells have bundles of thin fibers (the stereocilia)
that protrude from the apical cell surface and act as sensitive accelerometers;
as a result, the hair cells are excited by sound-induced vibrations in the inner
ear. This excitation produces electrochemical signals that are conducted by the
auditory nerve to the auditory centers in the brain in a process that we call
hearing [4,5].1
r The examples above show that biomechanics is important in homeostasis and
normal function. Unfortunately, biomechanics also plays a role in some dis-
eases. One example is glaucoma, an ocular disease that affects about 65 million
people worldwide [6]. Normally the human eye is internally pressurized, a fact
that you can verify by gently touching your eye through the closed eyelid. In
most forms of glaucoma, the pressure in the eye becomes elevated to patholog-
ical levels, and the resulting extra biomechanical load somehow damages the
optic nerve, eventually leading to blindness [7]. A second example is atheroscle-
rosis, a common arterial disease in which non-physiological stress distributions
on endothelial cells promote the disease process [8].
r What about biomechanics in the treatment of disease and dysfunction? There
are obvious roles in the design of implants that have a mechanical function,

1
Actually, the function of the hair cells is even more amazing than it first appears. The outer hair cells are active
amplifiers, changing their shape in response to mechanical stimulation and thus generating sounds. The net effect is to
apply a frequency-selective boost to incoming sounds and hence improve the sensitivity of the ear.
 3 1.1 A brief history of biomechanics

such as total artificial hips [9], dental implants [10], and mechanical heart
valves [11]. In the longer term, we expect to treat many diseases by implanting
engineered replacement tissue into patients. For tissues that have a mechanical
function (e.g., heart valves, cartilage), there is now convincing evidence that
application of mechanical load to the tissue while it is being grown is essential
for proper function after implantation. For example, heart valves grown in a
bioreactor incorporating flow through the valve showed good mechanical prop-
erties and function when implanted [12]. Cartilage subjected to cyclic shearing
during growth was stiffer and could bear more load than cartilage grown with-
out mechanical stimulation [13]. We expect that biomechanics will become
increasingly important in tissue engineering, along the way leading to better
fundamental understanding of how cells respond to stresses.

The above examples should give a flavor of the important role that biomechanics
plays in health and disease. One of the central characteristics of the field is that
it is highly interdisciplinary: to be called biomechanics, there must be elements
of both mechanics and biology (or medicine). Advances in the field occur when
people can work at the frontier of these two areas, and accordingly we will try to
give both the “bio” and the “mechanics” due consideration in this book.
Another characteristic feature of biomechanics is that the topic is fairly broad. We
can get a sense of just how broad it is by looking at some of the professional societies
that fall under the heading of biomechanics. For example, in Japan alone, at least
six different professional societies cover the field of biomechanics.2 Obviously we
cannot, in a single book, go into detail in every topic area within such a broad field.
Therefore, we have given an introduction to a variety of topics, with the hope of
whetting readers’ appetites.

1.1 A brief history of biomechanics

We can learn more about the field of biomechanics by looking at its history. In
one sense, biomechanics is a fairly young discipline, having been recognized as an
independent subject of enquiry with its own body of knowledge, societies, journals,
and conferences for only around 30–40 years. For example, the “Biomechanics and
Human Factors Division” (later to become the “Bioengineering Division”) of the
American Society of Mechanical Engineering was established in late 1966. The
International Society of Biomechanics was founded August 30, 1973; the European

2
These are the Japanese Society of Biomechanics, the Bioengineering Division of the Japan Society of Mechanical
Engineers, the Japan Society of Medical Electronics and Biological Engineering, the Association of Oromaxillofacial
Biomechanics, the Japanese Society for Clinical Biomechanics and the Japanese Society of Biorheology.
4 Introduction

Society of Biomechanics was established May 21, 1976, and the Japanese Society
of Biomechanics was founded December 1, 1984. On the other hand, people have
been interested in biomechanics for hundreds of years, although it may not have
been called “biomechanics” when they were doing it. Here we take a quick look
back through history and identify some of the real pioneers in the field. Note that
the summary below is far from exhaustive but serves to give an overview of the
history of the field; the interested reader may also refer to Chapter 1 of Fung [14]
or Chapter 1 of Mow and Huiskes [15].
Galileo Galilei (1564–1642) was a Pisan who began his university training in
medicine but quickly became attracted to mathematics and physics. Galileo was a
giant in science, who, among other accomplishments, was the first to use a tele-
scope to observe the night sky (thus making important contributions in astronomy)
and whose synthesis of observation, mathematics, and deductive reasoning firmly
established the science that we now call mechanics.3 Galileo, as part of his studies
on the mechanics of cantilevered beams, deduced some basic principles of how
bone dimensions must scale with the size of the animal. For example, he realized
that the cross-sectional dimensions of the long bones would have to increase more
quickly than the length of the bone to support the weight of a larger animal [17].
He also looked into the biomechanics of jumping, and the way in which loads are
distributed in large aquatic animals, such as whales. However, Galileo was really
only a “dabbler” in biomechanics; to meet someone who tackled the topic more
directly, we must head north and cross the English Channel.
William Harvey (1578–1657) was an English physician who made fundamen-
tal contributions to our understanding of the physiology of the cardiovascular
system, and who can be rightly thought of as one of the first biomechanicians
(Fig. 1.1). Before Harvey, the state of knowledge about the cardiovascular system
was primitive at best, being based primarily on the texts of the Roman physician
Galen (129–199?). Galen believed that the veins distributed blood to the body, while
arteries contained pneuma, a mixture of “vital spirits,” air, and a small amount of
blood. It was thought that the venous and arterial systems were not in communi-
cation except through tiny perforations in the interventricular septum separating
the two halves of the heart, so the circulatory system did not form a closed loop.
Venous blood was thought to be produced by the liver from food, after which it
flowed outward to the tissues and was then consumed as fuel by the body.4
Harvey was dissatisfied with Galen’s theories, and by a clever combination of
arguments and experimentation proved that blood must travel in a closed circuit
3
Charles Murray, in his remarkable survey of human accomplishment through the ages [16], ranks Galileo as the
second-most accomplished scientist of all time, behind (who else?) Newton.
4
It is easy to look back and ask: How could Galen have been so wrong? The answer is that he was influenced by his
predecessors; prior to Galen it was thought that arteries were filled with air and that the veins originated in the brain, for
example. The lesson to be learned: question dogma!
5 1.1 A brief history of biomechanics

Figure 1.1
Portraits of Drs. William Harvey (left) and Stephen Hales (right). Both were early biomechanicians; Harvey was a noted
English physician, while Hales was a Reverend and “amateur” scientist. Both portraits, courtesy of the Clendening
History of Medicine Library and Museum, University of Kansas Medical Center [18].

in the cardiovascular system. For example, he carried out careful dissections and
correctly noted that all the valves in veins acted to prevent flow away from the
heart, strongly suggesting that the function of the veins was to return blood to the
heart. For our purposes, his most intriguing argument was based on a simple mass
balance: Harvey reasoned that the volumetric flow of blood was far too large to be
supplied by ingestion of food. How did he do this? Using a sheep’s heart, he first
estimated the volume of blood pumped per heart beat (the stroke volume) as two
ounces of blood. Knowing the heart rate, he then computed that the heart must be
pumping more than 8600 ounces of blood per hour, which far exceeds the mass of
food any sheep would be expected to eat! In his words (italics added) [19]:

Since all things, both argument and ocular demonstration, show that the blood passes
through the lungs and heart by the force of the ventricles, and is sent for distribution to all
parts of the body, where it makes its way into the veins and porosities of the flesh, and then
flows by the veins from the circumference on every side to the center, from the lesser to the
6 Introduction

greater veins, and is by them finally discharged into the vena cava and right auricle of the
heart, and this in such a quantity or in such a flux and reflux thither by the arteries, hither
by the veins, as cannot possibly be supplied by the ingesta, and is much greater than can
be required for mere purposes of nutrition; it is absolutely necessary to conclude that the
blood in the animal body is impelled in a circle, and is in a state of ceaseless motion.

By these and additional arguments [20], Harvey deduced the closed nature of the
cardiovascular system (although he was unable to visualize the capillaries). For
our purposes, Harvey is notable because he was one of the first physicians to
use a combination of quantification, deductive reasoning, and experimentation to
understand a clinically important medical topic. Such approaches are commonplace
today but were revolutionary in Harvey’s time and even caused him to be strongly
criticized by many prominent physicians.
Giovanni Alfonso Borelli (1608–1679) is variously described as a mathemati-
cian, physicist, and physiologist, which is surely a testament to the breadth of
his interests. He worked at various universities throughout Italy, coming in con-
tact with Galileo. Notably, he spent 10 years in Pisa, where he worked with the
famous anatomist Malpighi (responsible for the discovery of the capillaries). Later
in his career, Borelli became interested in the mechanics of animal motion, and is
best known for his two-volume work on this topic, On the Movement of Animals
(De Motu Animalium), published posthumously in 1680 (Volume I) and 1681
(Volume II). In addition to the novelty of the material in these books, they are
notable for their wonderfully detailed figures illustrating biomechanical concepts
such as locomotion, lifting, and joint equilibrium (Fig. 1.2). Borelli used the princi-
ples of levers and other concepts from mechanics to analyze muscle action. He also
determined the location of the center of gravity of the human body and formulated
the theory that forward motion involved the displacement of the center of gravity
beyond the area of support and that the swinging of the limbs saved the body from
losing balance [21]. Further, he considered the motor force involved in walking and
the location of body support during walking. Borelli was also interested in respira-
tory mechanics: he calculated and measured inspired and expired air volumes. He
was able to show that inspiration is driven by muscles, while expiration is a passive
process resulting from tissue elasticity. In honor of his seminal contributions in the
field of biomechanics, the career accomplishment award of the American Society
of Biomechanics is known as the Borelli Award.
Another early biomechanician was the Reverend Stephen Hales (1677–1761),
who made contributions to both plant and animal physiology (Fig. 1.1). He is best
known for being the first to measure arterial blood pressure, now a staple of all
clinical examinations. He did this by direct arterial cannulation of his horse (in his
back yard, no less)! In his words [22,23]:
7 1.1 A brief history of biomechanics

Figure 1.2
Figure from Borelli’s classic work, De Motu Animalium (On the Movement of Animals). Panels 1–4 show how elastic
bands (representing muscles) can interact with two pivoting levers (representing bones) in a variety of geometric
configurations. Panels 5 and 6 demonstrate how the muscle and bone configurations act in humans carrying loads.
Panels 7 and 8 show various pulley arrangements, while panels 9 and 10 show how muscle action in the human arm
supports a weight R. (We will revisit this subject in Ch. 8.) The concepts may not seem advanced to modern students,
but to put things into context, it should be remembered that the first volume of De Motu Animalium was published seven
years before the appearance of Newton’s Principia.
8 Introduction

I caused a mare to be tied down alive on her back . . . having laid open the left crural
[femoral] artery about 3 inches from her belly, I inserted into it a brass pipe whose bore was
1/6 of an inch in diameter; and to that, by means of another brass pipe . . . I fixed a glass
tube of nearly the same diameter, which was 9 feet in length; then untying the ligature on
the artery, the blood rose in the tube 8 feet 3 inches perpendicular above the level of the
left ventricle of the heart . . . when it was at its full height, it would rise and fall at and after
each pulse 2, 3, or 4 inches.

Hales also improved Harvey’s estimate of cardiac stroke volume by pouring wax
at controlled pressure into the heart’s main pumping chamber (the left ventricle)
to make a casting. He then measured the volume of the wax cast by immersing it
in water, and measured its surface area by carefully covering it with small pieces
of paper covered with a measuring grid. Together with his measurements of blood
pressure, Hales then used these results to provide the first estimate of left ventric-
ular systolic (pumping) pressure, and a remarkably accurate estimate of the blood
velocity in the aorta (0.5 m/s).
Jean Léonard Marie Poiseuille (1797–1869; Fig. 1.3) was a French engineer
and physiologist who was also interested in blood flow [25]. In his thesis [27], he
described how he simplified and improved the measurement of blood pressure. His
contributions were two-fold: first, he developed the U-tube mercury manometer,
which did away with the need for an unwieldy 9 foot-long tube. Second, he used
potassium carbonate as an anticoagulant [28]. He was surprised to discover that
the pressure drop from the aorta to arteries with diameters as small as 2 mm was
negligible [29]; we know now that most of the pressure drop in the circulatory
system occurs in vessels with diameter smaller than 2 mm. Poiseuille then became
interested in laminar flow in small tubes and carried out experiments on the flow
of water through artificial glass capillaries with diameters as small as 30 μm. His
results allowed him to deduce the relationship between flow, tube dimensions, and
pressure drop, which we know today as the Hagen–Poiseuille law [30]. We will
explore the implications of this law for blood flow in Ch. 3.
Thomas Young (1773–1829) was an English physician and physicist (Fig. 1.3).
He was remarkably prodigious as a child, having learned to read “with considerable
fluency” at the age of two, and demonstrating a knack for languages, such that he
had knowledge of English, Greek, Latin, French, Italian, and Hebrew by the age
of 13 [26]. He studied medicine and practiced in London while developing and
maintaining expertise in a staggering range of areas. For example, he demonstrated
the wave theory of light, deciphered some of the first Egyptian hieroglyphics by
analysis of the Rosetta stone, helped to establish actuarial science, and lectured on
the theory of tides, surface tension, etc. In the biomedical area, he established, with
von Helmholtz, the theory of color, discovered and measured astigmatism in the
9 1.1 A brief history of biomechanics

Figure 1.3
Portraits of Drs. Jean Poiseuille (left) and Thomas Young (right). Both men did important work in physiology and
medicine, yet are familiar to engineering students: Poiseuille for his work on steady laminar incompressible flow in a
tube of uniform circular cross-section (Hagen–Poiseuille flow) and Young from his work on the elasticity of bodies
(Young’s modulus of elasticity). Poiseuille portrait reproduced with permission from [24] as modified by Sutera [25];
Young portrait by Sir Thomas Lawrence, engraved by G. R. Ward, as shown in Wood [26].

eye, and deduced that the focussing power of the eye resulted from changes in the
shape of the lens. He devised a device for measuring the size of a red blood cell, with
his measurements showing a size of 7.2 μm [26], a value that is remarkably accurate
(see Ch. 3). He also studied fluid flow in pipes and bends, and the propagation of
impulses in elastic vessels, and then applied this to analysis of blood flow in the
arteries. He correctly deduced that peristaltic motion of the artery wall did not
contribute to the circulation of blood, and instead that the motive power must
come from the heart [31]. He is most familiar to engineering students for defining
the modulus of elasticity, now known as Young’s modulus in his honor.
Julius Wolff (1836–1902) and Wilhelm Roux (1850–1924) were German physi-
cians (Fig. 1.4). Of the two, Wolff is better known to biomedical engineers because
10 Introduction

Figure 1.4
Portraits of Drs. Julius Wolff (left) and Wilhelm Roux (right). Both were German physicians who were interested in how
mechanical forces could influence the structure and development of bone. Both portraits, courtesy of the Clendening
History of Medicine Library and Museum, University of Kansas Medical Center [18].

of his formulation of “Wolff’s law” of bone remodeling. Legend has it [32] that the
structural engineer Karl Culmann saw a presentation by the anatomist Hermann
von Meyer, in which von Meyer described the internal architecture of the bone in
the head of the femur. Culmann was struck by the similarity between the pattern
of solid elements in the cancellous (“spongy”) bone of the femur and the stress
trajectories5 in a similarly shaped crane that he was designing (Fig. 1.5).6 Based
on von Meyer’s paper describing this similarity [33], as well as other data avail-
able at the time, Wolff hypothesized that bone was optimized to provide maximum
strength for a minimum mass. He then went on to formulate his “law” of bone

5
A stress trajectory is an imaginary line drawn on a surface that is everywhere tangent to the principal stress directions on
the surface. Stress trajectories help to visualize how the stress is carried by an object, and they can be used as the basis
of a graphical procedure for determining stress distributions in bodies. This graphical solution method is now obsolete,
having been replaced by computational methods.
6
This certainly emphasizes the importance of interdisciplinary interaction in biomedical engineering!
11 1.1 A brief history of biomechanics

Figure 1.5
Comparison of internal architecture of cancellous bone in the head of a femur (large drawing at right) and the stress
trajectories in the head of a crane (large drawing at left). The smaller drawings provide details of the mechanics of the
crane and the stress distributions in various structures. This picture originally appeared in the article by von Meyer [33],
as reproduced in [32].

remodeling [34,35]:7 “Every change in the form and the function of a bone or of
their function alone is followed by certain definite changes in their internal archi-
tecture, and equally definite secondary alterations in their external confirmation,
in accordance with mathematical laws.” In simpler terms, Wolff stated that bone
will adapt its internal architecture in response to external constraints and loads.
Wolff went on to claim a rigorous similarity between cancellous bone architecture
and stress trajectories. Cowin has shown that this is based on a false comparison of
apples and oranges (i.e., a continuous material vs. a porous one) [32] and argued
persuasively that Wolff gets rather too much credit for his remodeling law, possi-
bly because he was a more prolific writer on this topic. Cowin [32] suggested that
the anatomist Roux should get at least as much credit as Wolff for this “law” of

7
Wolff’s original book was in German [34], but an English translation exists [35].
12 Introduction

remodeling, and we are inclined to agree. Roux was very interested in developmen-
tal biology and physiology, carrying out his doctoral work on the factors governing
the bifurcation of blood vessels [36]. He was convinced that mechanical and phys-
ical principles played important roles in development (e.g., [37]) and carried out
seminal experimental studies in this area. In 1894, he also founded a journal enti-
tled Archiv für Entwicklungsmechanik (Archives of Developmental Mechanics) and
served as its editor for many years, stirring up his fair share of controversy along the
way [38]. He may be rightly thought of as the first developmental biomechanician.
In the years since Wolff and Roux, there have been many advances in biome-
chanics. This is not the place to try to provide a complete history of biomechanics,
and we will not list all of the outstanding investigators who have worked (or are
working) in this fast-growing field. However, it is worth mentioning one other
investigator. An important event in the maturation of the field of biomechanics
was the publication, in 1981, of the book Biomechanics: Mechanical Properties
of Living Tissues, by Yuan-Cheng Fung (Fig. 1.6). Fung was born in 1919 and
was trained as an aeronautical engineer, a field in which he made many techni-
cal contributions in the early years of his career. However, in the late 1950s, he
became interested in biomechanics and consequently changed his research focus
away from aeronautics. In addition to his 1981 book, Fung has also written sev-
eral other books in biomechanics [40,41]. Y.-C. Fung is generally regarded as the
“father” of modern biomechanics and has the rare distinction of being a member
of the US National Academy of Engineering, the US Institute of Medicine, and
the US National Academy of Sciences. Membership in all three of these learned
societies is surely a testament to the abilities of Dr. Fung, but it is also a reflection of
the highly interdisciplinary nature of biomechanics, which (when done properly)
should tightly integrate engineering, medicine, and biology.

1.2 An outline of this book

Western science is traditionally reductionist: we tend to conceptually break down

complex systems into smaller functional units, and try to analyze those units and
their interconnectivity (although see the aside on systems biology below). We will
follow this approach in this book because we believe that this is the best way for
the student to be introduced to a topic.
The basic unit of life is the cell, and an understanding of cellular behavior
is a cornerstone of modern bioengineering. In Chapter 2, we describe the basic
components of the cell, with special emphasis on molecules that play a role
in the biomechanical behavior of the cell. We then attempt to synthesize our
understanding of these molecular components to answer basic questions about
13 1.2 An outline of this book

Figure 1.6
Portrait of Y.-C. Fung, who has played an important role in the establishment of biomechanics as a modern, rigorous
discipline, primarily through the publication of an influential series of books on biomechanics. Reproduced with
permission from [39].

cellular biomechanics. How stiff is a cell, and how do we measure this parameter?
How does the cell anchor itself to substrates and to neighbors? How does the
cell respond to external forces, and what implications does this have for tissue
organization?
At a higher level, physiologists subdivide the body into organs, which are tissues
specialized for a specific purpose, and systems, which are collections of organs
working in concert. In this book, we will also consider the biomechanics of some
of the body’s systems. There are many such systems; here is a partial list and
description of their functions, with emphasis on the biomechanical aspects.

Circulatory system. This system delivers nutrients and picks up waste products
from the cells, as well as delivering signaling molecules, such as hormones, between
different organs. The flow of blood will be studied in Ch. 3; other biomechanical
aspects of the circulatory system are discussed in Ch. 4.
14 Introduction

Lymphatic system. Excess fluid is passively collected from tissues and returned
to the heart via a network of ducts and channels that make up the lymphatic system.
The lymphatic system is also an important locus for immune function. We will
not examine the lymphatic system in detail, although it is briefly touched upon
in Ch. 5.
Nervous and sensory systems. The nervous system consists of the nerves and
brain and is responsible for signaling and control within the body. Its operation
is highly complex and will not be considered in this book. The sensory organs
provide input to the nervous system; we will briefly consider ocular biomechanics
in Ch. 6.
Respiratory system. In order to oxidize foodstuffs, O2 must be delivered to the
blood and CO2 must be removed from it. This is accomplished by exposing the
blood to the air through a very thin membrane of enormous surface area. This
membrane is convoluted and folded to form a large number of small sacs within
the lung. The respiratory system consists of the lungs, plus structures that assist
air passage in and out of the lungs. It will be considered in Ch. 7.
Urinary system. The urinary system consists of the kidneys, ureters, urinary
bladder, and urethra. The kidneys are responsible for removing waste products
from blood and for the production of urine, which is then stored in the bladder and
excreted through the urethra. The biomechanics of the urinary system is fascinating
and complex [42–45]. Unfortunately, consideration of the urinary system is beyond
the scope of this book.
Muscular system. Muscles are specialized tissues that generate force upon
appropriate stimulation. Muscular action is required for locomotion (movement
of the body), motion of individual body parts, and bulk transport of materials
within the body (e.g., pumping of blood by the heart). Muscles, and how they
effect motion, will be discussed in Chs. 8 and 10.
Skeletal system. This framework of bones and soft connective tissues (cartilage,
ligaments, and tendons) provides a rigid, supportive, and protective structure for the
body. The bony skeleton also provides attachments for muscles, serves as a system
of levers for movement and locomotion, and has important metabolic functions.
Bones, cartilage, ligaments, and tendons will be discussed in greater detail in
Ch. 9.
Digestive system. The digestive system comprises the gastrointestinal tract
(mouth to anus) plus the liver, gall bladder, and pancreas. The digestive system
is responsible for ingestion and breakdown of food, delivery of foodstuffs to the
blood, and waste excretion. We will not consider the digestive system in this book.
Immune system. This system consists of specialized cells and molecules dis-
tributed throughout the body (in organs such as the spleen and as cells in the blood-
stream and interstitial fluid). It is responsible for identification and destruction of
15 References

foreign entities, including viruses and bacteria. Consideration of the immune sys-
tem is beyond the scope of this book.

Box 1.1 Systems biology and the integration of information

The reductionist trend in biology has begun to change recently, with the
emergence of several high-profile initiatives in systems biology. The goal
here is to integrate information at the genomic, protein, and higher levels to
understand how biological systems work as functional units. A wonderful
example of a systems biology approach is the work of Davidson and
coworkers [46], who are mapping the genetic regulatory network in the
sea urchin (Strongylocentrotus purpuratus) embryo. By using a variety
of techniques, including perturbing the function of regulatory genes and
observing their effects on embryo development, they have produced maps
of genetic regulatory networks that convey a taste of the complexity of life
(Fig. 1.7 [color plate]; note this represents the development of only part of the
sea urchin embryo, for a small fraction of the developmental period). Readers
will note that there are no biomechanical stimuli listed in this diagram; these
have yet to be elucidated.

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16 Introduction

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17 References

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33. G. H. von Meyer. Die Architektur Der Spongiosa. Archiv für Anatomie, Physiologie
und Wissenschaftliche Medizin, 34 (1867), 615–628.
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2 Cellular biomechanics

The cell is the building block of higher organisms. Individual cells themselves
are highly complex living entities.1 There are two general cell types: eukaryotic
cells, found in higher organisms such as mammals, and prokaryotic cells, such as
bacteria. In this chapter, we will examine the biomechanics of eukaryotic cells only.
We will begin by briefly reviewing some of the key components of a eukaryotic cell.
Readers unfamiliar with this material may wish to do some background reading
(e.g., from Alberts et al. [1] or Lodish et al. [2]).

2.1 Introduction to eukaryotic cellular architecture

Eukaryotic cells contain a number of specialized subsystems, or organelles, that

cooperate to allow the cell to function. Here is a partial list of these subsystems.

Walls (the membranes). These barriers are primarily made up of lipids in a bilayer
arrangement, augmented by specialized proteins. They serve to enclose the cell,
the nucleus, and individual organelles (with the exception of the cytoskeleton,
which is distributed throughout the cell). The function of membranes is to create
compartments whose internal materials can be segregated from their surroundings.
For example, the cell membrane allows the cell’s interior to remain at optimum
levels of pH, ionic conditions, etc., despite variations in the environment outside
the cell. The importance of the cell membrane is shown by the fact that cell death
almost invariably ensues if the cell membrane is ruptured to allow extracellular
materials into the cell.
A framework (the cytoskeleton). This organelle consists of long rod-shaped
molecules attached to one another and to other organelles by connecting molecules.

1
What defines a living system? A living system must satisfy the following five characteristics:
r it must show complex organization (specialization)
r it must be able to metabolize (assimilate “food,” transform it, and excrete it)
r it must show responsiveness, including the ability to adapt to differing conditions
r it must be able to reproduce
r it must have evolutionary capability.
Individual cells exhibit each of these characteristics.
19 2.1 Introduction to eukaryotic cellular architecture

The cytoskeleton gives the cell form, allows it to move, helps to anchor the cell to its
substrate and neighbors, and speeds the transport of materials within certain types
of cells. We will consider the cytoskeleton in greater detail later in this chapter.
Engines (the mitochondria). These organelles produce most of the basic energy-
containing molecules from certain substrates such as glucose. Then these energy-
containing molecules are used by other subsystems within the cell.
A command center (the nucleus). The genetic material which codes for
molecules synthesized by the cell is mostly contained in the nucleus, although
there is a small amount of mitochondrial DNA. The synthesis of proteins and other
important biomolecules is initiated by transcription of genetic information coded
in DNA into messenger RNA (mRNA). These mRNA coding sequences leave the
nucleus where they are eventually turned into proteins by . . .
Factories (the endoplasmic reticulum). These production centers synthesize
biomolecules needed by the cell. They take their “orders” from the nucleus in
the form of mRNA.
Packaging plants (the Golgi apparatus). Proteins produced by the endoplasmic
reticulum are not “ready for prime time.” They typically must undergo a series
of folding steps and post-translational modifications before they have biologi-
cal activity. This very important task is handled by the Golgi apparatus, which
takes the protein output of the endoplasmic reticulum and trims, modifies, and
packages it in membrane-delimeted structures (the vesicles) that are sent to var-
ious locations within or outside the cell. Misfolded and otherwise defective pro-
teins must be disposed of immediately since they are potentially harmful to the
cell.
A disposal system (the lysozomes). This system of vesicles contains enzymes
(catalytic proteins) which act to break down metabolic by-products, misfolded
proteins, ingested extracellular material, and other unwanted substances.

Clearly a single cell is a remarkable assortment of complex subsystems (Figs. 2.1

and 2.2). It is also a miracle of miniaturization: all of the above systems fit into a
neat package having a typical mass of 2 × 10−8 g, and a typical diameter of order
15 μm!
Now that we have a basic overview of the components of a eukaryotic cell, let
us look in more detail at cellular biomechanics and mechanobiology. We will start
(Section 2.2) with some basic ideas about how the cell uses energy, which we will
see resembles energy flow in a thermal energy-generating station in some ways.
Then we will delve into more detail about the cytoskeleton of the cell, focussing
on its mechanical properties and how it helps to anchor the cell to its surroundings
(Sections 2.3 and 2.4). The main focus here will be to give the reader enough
biological background to understand Sections 2.5 and onwards.
 20 Cellular biomechanics

Microfilaments
Plasma membrane

Secretory vesicle

Microtubule
Lysosome

Centrioles
Peroxisome

Golgi apparatus Mitochondrion

Free ribosome

Nucleus
Bound ribosome
Nucleolus
Granular
endoplasmic
reticulum Nuclear envelope

Nuclear pore

Agranular
endoplasmic
reticulum

Figure 2.1
Structures and organelles found in most human cells. This diagram is highly schematized but serves to indicate the
major features of the cellular organelles. From Vander et al. [3]. Reproduced with kind permission of the McGraw-Hill
Companies.

When engineers talk about the mechanics of conventional engineering materials,

they can refer to handbooks that tabulate the properties of, for example, different
types of stainless steel, and describe the internal structure of these steels. Can
we do that for cells? Not quite, but a body of data is slowly being accumulated
about the “mechanical properties of cells.” In Section 2.5, we will tackle the tricky
question of how one measures the mechanical properties of a single cell, while in
Section 2.6 we will introduce some engineering models that, in combination with
experimental data, teach us something about the cell’s internal mechanics.
21 2.1 Introduction to eukaryotic cellular architecture

Figure 2.2
Transmission electron micrograph of an insulin-producing pancreatic cell, showing several of the structures depicted
schematically in Fig. 2.1. A prominent nucleus delimited by the nuclear envelope (membrane) is present, as are several
organelles in the cytoplasm: mitochondria, Golgi complex, and endoplasmic reticulum with associated ribosomes. A
second cell is visible at the top left of the image. Sample stained with uranyl acetate and lead citrate. Micrograph
courtesy of Mr. Steven Doyle, University of Toronto.

One of the remarkable things about most cells is how good they are at sens-
ing relatively small levels of mechanical stimulation, while living in a constantly
changing biomechanical environment. How do they do this? Many details of this
process, known as mechanotransduction, are unknown, but in Section 2.7 we will
discuss, in general terms, current thinking on how adherent cells are able to sense
and respond to mechanical stimulation.
22 Cellular biomechanics

Finally, we consider the consequences of the response of cells to mechanical

stimulation. In Section 2.8, we describe some of the experimental tools that are
used to apply mechanical stimuli to tissues or small groups of cells in culture.
Using these devices, the effects of mechanical stimulation on several cell types
have been determined. In Section 2.9, we present some of the effects on cells from
three specific tissues (vascular tissue, cartilage, and bone) and we consider the
implications for the whole tissue. Let’s get started!

2.2 The cell’s energy system

Life requires energy. At the cellular level, energy-consuming tasks include:

r motion, including both cellular shape changes and locomotion of the cell on its
substrate
r synthesis of compounds
r transport of ions and other molecules, both within the cell and between the cell
and its surroundings

How does the cell utilize food energy? When we eat a meal, the constituent food-
stuffs are acted upon by the digestive enzymes and broken down into simpler
compounds, transferred into the bloodstream across the intestinal walls, and then
transported throughout the body.
Individual cells are therefore presented with a complex mixture of compounds
from which they must obtain energy. The cell solves this problem by having spe-
cialized “energy plants” (mitochondria), which are able to use compounds such
as glucose and fatty acids to produce a common energy-containing molecule that
all cellular organelles can use. This common molecule is adenosine triphosphate
(ATP), formed from adenosine diphosphate (ADP) and phosphate (PO2− 3 ) in the
following reaction:
+
ADP + PO2−
3 + energy + 2H → ATP

Energy is stored in the chemical bond between ADP and PO2− 3 (Fig. 2.3). A mechan-
ical analogue is a spring, which starts in an uncompressed state (ADP) and is then
compressed and held in place by a catch (PO2− 3 ). The organelles can “release the
catch” to produce energy, with by-products ADP and PO2− 3 . We say, therefore, that
ATP is the common currency of energy within the cell.
It is important to note that ADP and phosphate are recycled, to be once more
combined in the mitochondria to yield ATP. This is similar to the movement of
primary loop cooling water in a thermal generating station, and it emphasizes that
ATP is merely a transient carrier of energy within the cell (Fig. 2.4).
23 2.3 Overview of the cytoskeleton

NH2

N C C
N adenine
CH
C CH
N N O O O
O CH2 O P O P O P O− + HOH
C H H C O− O− O−
H C C
OH OH
Ribose
ATP

NH2

N C C
N
CH
CH
N C N O O O
O CH2 O P O P O− + HO P O− + H+ + 7 kcal/mole
C H H C O− O− O−
H C C H Inorganic phosphate
OH OH

ADP

Figure 2.3
Structure of ADP and ATP. The breakdown of ATP to ADP and inorganic phosphate yields 7 kcal/mole energy. From
Vander et al. [3]. Reproduced with kind permission of the McGraw-Hill Companies.

2.3 Overview of the cytoskeleton

Just as an understanding of a cell’s architecture and its energy system is critical to

understanding cellular biology, the characteristics of the cytoskeleton are central to
understanding a cell’s biomechanical behavior. Here we will only give an overview
of this fascinating topic. Students are encouraged to consult the references if they
wish to learn more about the cytoskeleton.
The cytoskeleton is an elaborate network of fibrous proteins that can adopt a
remarkable range of configurations (Figs. 2.5 and 2.6). It:
r establishes and maintains the shape of the cell
r allows the cell to move (the process of locomotion)
24 Cellular biomechanics

Primary Loop Secondary Loop

Water + steam To
Fuel + turbines
oxygen

Burner + Secondary Heat

Primary Heat Exchanger
Exchanger

Return
from
CO2 +
Water turbines
H2O

Energy Flow

Carbohydrates, Organelle
ATP
protein, fats + products
oxygen

Mitochondria Organelles

CO2 + Raw
H2O ADP + PO32− materials

Figure 2.4
Energy flow in a thermal generating station (top) and a cell (bottom). Note that primary loop cooling water is analogous
to ATP in that it is a transient vehicle for energy storage which is recycled.

r provides mechanical strength and integrity to the cell

r is central to the intracellular transport of organelles, especially in large cells
such as axons
r is essential during cell division, where it plays a key role in many processes,
including chromosome separation in mitosis and meiosis.

The cytoskeleton consists of three types of filament, each with a specialized pro-
tein composition: actin filaments (7–9 nm in diameter), intermediate filaments
(10 nm in diameter), and microtubules (approximately 24 nm in diameter). Actin
filaments are also called microfilaments or – in skeletal muscle cells – thin fila-
ments. The interaction between all three filament types helps to determine the cell’s
mechanical behavior. We will briefly review the function of each of these filament
types.
 25 2.3 Overview of the cytoskeleton

Figure 2.5
Scanning electron micrograph of the actin component of the cytoskeleton within a rat fibroblast adhering to an
N-cadherin-coated glass cover slip (A). A high-magnification inset of the boxed region is shown in (B). The rich, highly
interconnected actin network is clearly visible. Cells were extracted with a detergent solution, fixed in glutaraldehyde,
post-fixed, and gold sputter coated before visualization. Images courtesy of Dr. Tarek El Sayegh, Faculty of Dentistry,
University of Toronto.

2.3.1 Actin filaments

Actin exists within the cell in two forms, as a globular protein (G-actin) and as
a filamentous protein (F-actin). G-actin has a molecular weight of approximately
43 kDa, and consists of a single polypeptide chain. Monomeric G-actin binds one
Ca2+ and one molecule of ATP. F-actin is formed by the polymerization of G-actin,
which causes the bound ATP to be hydrolyzed to ADP and a phosphate ion (Fig. 2.7,
color plate). The ADP remains bound to the actin subunit within the F-actin chain.
F-actin chains are dynamic structures that grow and break down according to
their position within the cell and the activities of the cell at any given instant. F-actin
filaments are polarized, having an end where G-actin monomers are preferentially
added (the fast-growing “barbed” or “+” end) and an end where the filament is
either slowly growing or disassembled (the “pointed” or “–” end). Thus, individ-
ual actin monomers move along filaments, tending to be added at the + end and
26 Cellular biomechanics

Figure 2.6
Cytoskeleton of the brush border of intestinal epithelial cells. Tight actin filaments are evident in the microvilli, the
finger-like structures in the top half of the image. The actin extends from microvilli into the cytoplasm of the cell, where it
connects with a network of actin, intermediate filaments, myosin, and other cytoskeletal proteins. The scale bar in the
lower left corner is 0.1 μm. Reproduced with permission from Bershadsky and Vasiliev [4] and from the Journal of Cell
Biology, 1982, 94, 425–443 by copyright permission of the Rockefeller University Press.
27 2.3 Overview of the cytoskeleton

Table 2.1. Summary of Young’s modulus values for F-actin measured

by various methods. Modified with permission from Janmey et al. [13].

Authors Method Estimated Young’s

modulus (N/m2 )

Kojima et al. [9] Micro-needle/single filament 1.8 × 109

Huxley et al. [10] X-ray diffraction frog/muscle 2.5 × 109
Higuchi et al. [11] Optical diffraction/rabbit Not in paper, by
skeletal muscle fiber comparison: ∼2 × 109
Wakabayashi X-ray diffraction/frog muscle Not in paper, by
et al. [12] comparison: ∼2 × 109

moving to the – end, in a process known as treadmilling (Fig. 2.8, color plate).
The polymerization and breakdown of F-actin are regulated by several proteins,
including actin depolymerizing factor/cofilin, members of the gelsolin/villin pro-
tein family, and CapZ. The lifetime of actin filaments, the length of the filaments,
the percentage of actin in polymeric form, and the number of barbed ends change
as a function of the cell’s activity. For example, in confluent bovine aortic endothe-
lial cells, the mean filament lifetime is approximately 40 min and about 70% of
the cell’s total actin is present as F-actin [8]. Confluent cells tend to be relatively
quiescent, exhibiting only modest amounts of cellular movement. In contrast, in
subconfluent endothelial cells, which are more active, the mean filament lifetime
is only approximately 8 min and only approximately 40% of the cell’s actin is
present in polymerized form [8].
F-actin exists within the cell in several different forms. In all cells, it is present
in a thin layer adjacent to the cell membrane, in the so-called cortical actin layer.
This layer helps to anchor transmembrane proteins to cytoplasmic proteins (see
Section 2.4) and generally provides mechanical strength to the cell. It also anchors
the centrosomes at opposite ends of the cell during mitosis, and helps the cell to split
into two parts during cytokinesis. In many cells, actin is also present in long bundles
that criss-cross the cell, known as stress fibers. Stress fibers presumably reinforce
the cortical actin layer and are also important for the transport of organelles and
cellular locomotion. Finally, in skeletal muscle cells, actin is highly abundant
and interacts with myosin filaments (thick filaments) to create the actin–myosin
complex, responsible for muscle contraction.
Because of its biomechanical importance, a number of authors have experimen-
tally estimated the Young’s modulus of F-actin filaments. Some of these measure-
ments are summarized in Table 2.1, which shows a fairly tight range of values of
order 2 GPa, approximately 100 times less than the modulus for steel.
Another Random Scribd Document
with Unrelated Content
ff. ) that besides the twelve, Jesus chose other seventy also, and
sent them two and two before him into all the districts which he
intended to visit on his last journey, that they might proclaim the
approach of the kingdom of heaven. As the other Evangelists have
no allusion to this event, the most recent critics have not hesitated
to make their silence on this head a reproach to them, particularly to
the first Evangelist, in his supposed character of apostle. 69 But the
disfavour towards Matthew on this score ought to be moderated by
the consideration, that neither in the other gospels, nor in the Acts,
nor in any apostolic epistle, is there any trace of the seventy
disciples, who could scarcely have passed thus unnoticed, had their
mission been as fruitful in consequences, as it is commonly
supposed. It is said, however, that the importance of this
appointment lay in its significance, rather than in its effects. As the
number of the twelve apostles, by its relation to that of the tribes of
Israel, shadowed forth the destination of Jesus for the Jewish
people; so the seventy, or as some authorities have it, the seventy-
two disciples, were representatives of the seventy or seventy-two
peoples, with as many different tongues, which, according to the
Jewish and early Christian view, formed the sum of the earth’s
inhabitants, 70 and hence they denoted the universal destination of
Jesus and his kingdom. 71 Moreover, seventy was a sacred number
with the Jewish nation; Moses deputed seventy elders (Num. xi.
16 , 25 ); the Sanhedrim had seventy members; 72 the Old
Testament, seventy translators.

Had Jesus, then, under the pressing circumstances that mark his
public career, nothing more important to do than to cast about for
significant numbers, and to surround himself with inner and outer
circles of disciples, regulated by these mystic measures? or rather, is
not this constant preference for sacred numbers, this assiduous
development of an idea to which the number of the apostles
furnished the suggestion, wholly in the spirit of the primitive
[333]Christian legend? This, supposing it imbued with Jewish
prepossessions, would infer, that as Jesus had respect to the twelve
tribes in fixing the number of his apostles, he would extend the
parallel by appointing seventy subordinate disciples, corresponding
to the seventy elders; or, supposing the legend animated by the
more universal sentiments of Paul, it could not escape the
persuasion that to the symbol of the relation of his office to the
Israelitish people, Jesus would annex another, significative of its
destination for all the kindreds of the earth. However agreeable this
class of seventy disciples may have always been to the church, as a
series of niches for the reception of men who, without belonging to
the twelve, were yet of importance to her, as Mark, Luke and
Matthew; we are compelled to pronounce the decision of our most
recent critic precipitate, and to admit that the Gospel of Luke, by its
acceptance of such a narrative, destitute as it is of all historical
confirmation, and of any other apparent source than dogmatical
interests, is placed in disadvantageous comparison with that of
Matthew. We gather, indeed, from Acts i. 21 f. that Jesus had more
than the twelve as his constant companions; but that these formed a
body of exactly seventy, or that that number was selected from
them, does not seem adequately warranted 73. [334]

Kuinöl, Comm. in Matth., s. 100; Lücke, Comm. z. Joh. 1, s. 388; Olshausen,

1
bibl. Comm. 1, s. 197; Hase, Leben Jesu, §§ 56, 61. ↑
Leben Jesu, 1, a, s. 212. ↑
2
Paulus, Leben Jesu, 1, a, s. 213; Sieffert, über den Ursprung u. s. f., s. 72. ↑
3
See Fritzsche, in Matt., p. 189. ↑
4
Schöttgen, horæ, ii. p. 372. ↑
5
 Paulus, ut sup. ↑
6
Paulus, exeg. Handb. 1, b, s. 464. ↑
7
Gnomon, in loc. ↑
8
Paulus, Leben Jesu, 1, a, s. 168. ↑
9
S. 385. ↑
10
Vid. Lücke, s. 389 f. ↑
11
Ut sup. ↑
12
P. 141. ↑
13
Storr, üeber den Zweck der ev. Gesch. und der Br. Joh.,
14
s. 350. ↑
Exeg. Handb. 1, b, s. 449. ↑
15
Bibl. Comm. 1, p. 283. ↑
16
Ueber den Lukas, s. 70. ↑
17
This, with the legendary character of both narratives, is acknowledged
18
by De Wette, exeg. Handb. 1, 1, s. 37, 1, 2, s. 38 f. ↑
Neander is of the same opinion, L. J., s. 249 f. ↑
19
Uber den Ursprung des ersten kan. Ev., s. 73. ↑
20
Berliner Jahrbücher für wissenschaftliche Kritik, 1834 Nov.; now in the
21
Charakteristiken u. Kritiken, s. 264 f. ↑
According to De Wette, the copious draught of fishes was a symbolical miracle,
22
typifying the rich fruits of the apostolic ministry. ↑
Porphyr. vita Pythagoræ, no. 25, ed. Kiessling; Jamblich. v. P. no. 36. ders.
23
Ausg. It is fair to adduce this history, because, being less marvellous than the
gospel narrative, it can hardly be an imitation, but must have arisen
independently, and hence it evinces a common tendency of the ancient legend. ↑
Luke v. 5 : δι’ ὅλης τῆς νυκτὸς κοπιάσαντες οὐδὲν ἐλάβομεν. John xxi. 3 : καὶ
24
ἐν ἐκείνῃ τῇ νυκτὶ ἐπίασαν ουδέν. ↑
Comp. de Wette, exeg Handb., 1, 3, s. 213. ↑
25
Vid. Kuinöl, in Matth., p. 255. ↑
26
 Sieffert, ut sup. p. 55. ↑
27
Kuinöl, ut sup. Paulus, exeg. Handb., 1, b, s. 513. L. J., 1, a, 240. ↑
28
Bertholdt, Einleitung, 3, s. 1255 f. Fritzsche, s. 340. ↑
29
Sieffert, s. 56; De Wette, exeg. Handb., 1, 1, s. 91. ↑
30
Sieffert, s. 60. ↑
31
De Wette, ut sup. ↑
32
Exeg. Handb., 1, b, s. 510. L. J., 1, a, 240. ↑
33
Schleiermacher, über den Lukas, s. 76. ↑
34
Grätz, Comm. z. Matth. 1, s. 470. ↑
35
Augustin c. Faust. Manich. xvii. 1. ↑
36
iii. i. 4. ↑
37
Plutarch. de gloria Atheniens., at the
38
beginning. ↑
Schulz, Ueber das Abendmahl, s. 308. ↑
39
Comp. de Wette, exeg. Handb. 1, 2, p. 134. ↑
40
Ut sup., p. 77. ↑
41
De Wette, exeg. Handb. I, 1, p. 93. ↑
42
Paulus, exeg. Handb., 3, a, s. 48. Kuinöl, in Luc., p. 632. ↑
43
Schleiermacher, über den Lukas, s. 85. ↑
44
Schleiermacher, über den Lukas, s. 85. ↑
45
Ut sup., s. 88. ↑
46
Ep. Barnab. 8, and the Gospel of the Ebionites ap.
47
Epiphanius, hær. xxx. 13. ↑
Schleiermacher, ut sup. s. 87. ↑
48
If ἡ πόλις Ἀνδρέου καὶ Πέτρου, John i. 45 , mean the same as ἡ ἰδία πόλις,
49
Matth. ix. 1 , that is, the place where they were resident, there exists a
contradiction on this point between John and the synoptists. ↑
Comp. Fritzsche, in Matt., p. 358. ↑
50
 Comp. Lightfoot, in loc. ↑
51
Comp. Saunier, über die Quellen des Markus, s. 55 f. ↑
52
Comp. de Wette, in loc. ↑
53
Paulus, exeg. Handb. 1, b, s. 556. ↑
54
This is probably a mere inference of Mark. Because Jesus excluded
55
the multitude, and forbade the publication of the event, the
Evangelist saw in it one of those secret scenes, to which Jesus was accustomed to
admit only the three favoured apostles. ↑
In the ancient church it was thought that Jesus had communicated to these
56
three individuals the γνῶσις, to be mysteriously transmitted. Vid. in Gieseler,
K. G. 1, s. 234. ↑
Even Paulus, L. J. 1, a, s. 167 f., remarks that the fourth Evangelist seems to
57
have had a design in noticing this circumstance. ↑
This has not escaped the acumen of Dr. Paulus. In a review of the first volume
58
of the second ed. of Lücke’s Comm. zum Johannes, in Lt. Bl. zur allg.
Kirchenzeitung, Febr., 1834, no. 18, s. 137 f., he says: “The gospel of John has
only preserved the less advantageous circumstances connected with Peter
(excepting vi. 68 ), such as place him in marked subordination to John [here the
passages above considered are cited]. An adherent of Peter can hardly have had a
hand in the Gospel of John.” We may add that it seems to have proceeded from an
antagonist of Peter, for it is probable that he had such of the school of John, as
well as of Paul. ↑
Vid. Lücke, Comm. zum Joh. 2, s. 708. ↑
59
Paulus, in his review of Bretschneider’s Probabilien, in the Heidelberger
60
Jahrbüchern, 1821, no. 9, s. 138. ↑
Lücke, ut sup. s. 664. ↑
61
Bretschneider, Probabilia, p. 111 f. ↑
62
Comp. Paulus, ut sup. s. 137. ↑
63
Thus most of the expositors, Fritzsche, Matth., s. 359; Winer,
64
Realwörterb. 1, s. 163 f. Comp. De Wette, exeg. Handb. 1, 1, s. 98. ↑
Joseph., bell. jud. iv. iii. 9. ↑
65
 Comp. Credner, Einleitung 1, s. 64; De Wette, exeg. Handb. 1, 1, s. 98 f. ↑
66
De Wette, ut sup. ↑
67
Ueber den Lukas, s. 88 f. ↑
68
Schulz, über das Abendmahl, s. 307; Schneckenburger, über den
69
Ursprung, s. 13 f. ↑
Tuf haarez, f. xix. c. iii.; Clem. hom. xviii. 4; Recognit. Clement. ii. 42; Epiphan.
70
hær. i. 5. ↑
Schneckenburger, ut sup.; Gieseler, über Entstehung der schriftl. Evangelien, s.
71
127 f. ↑
Lightfoot, p. 786. ↑
72
De Wette, exeget. Handb., 1, 1, s. 99 f. 1, 2, s. 61. 1, 3, s. 220; Theile, zur
73
Biogr. J., § 24. For the contrary opinion, see Neander, L. J. Chr., s. 498 f. ↑
[Contents]
CHAPTER VI.
 THE DISCOURSES OF JESUS IN THE THREE FIRST
GOSPELS. 1
[Contents]

§ 76.

THE SERMON ON THE MOUNT.

In reviewing the public life of Jesus, we may separate from the

events those discourses which were not merely incidental, but which
stand independent and entire. This distinction, however, is not
precise, for many discourses, owing to the occurrences that
suggested them, may be classed as events; and many events, from
the explanations annexed to them, seem to range themselves with
the discourses. The discourses of Jesus given in the synoptical
gospels, and those attributed to him in the fourth, differ widely both
in form and matter, having only a few isolated sentences in common:
they must, therefore, be subjected to a separate examination. Again,
there is a dissimilitude between the three first Evangelists: Matthew
affects long discourses, and collects into one mass a number of
sayings, which in Luke are distributed among various places and
occasions; each of these two Evangelists has also some discourses
peculiar to himself. In Mark, the element of discourses exists in a
very small proportion. Our purpose will, therefore, be best
answered, if we make Matthew’s comprehensive discourses our
starting point; ascertain all the corresponding ones in the other
gospels; inquire which amongst them has the best arrangement and
representation of these discourses; and, finally, endeavour to form a
judgment as to how far they really proceeded from the lips of Jesus.

The first long discourse in Matthew is that known as the Sermon on

the Mount (v.–vii. ). The Evangelist, having recorded the return of
Jesus after his baptism into Galilee, and the calling of the fishermen,
informs us, that Jesus went through all Galilee, teaching and
healing; that great multitudes followed him from all parts of
Palestine; and that for their instruction he ascended a mountain, and
delivered the sermon in question (iv. 23 ff. ). We seek in vain for its
parallel in Mark, but Luke (vi. 20–49 ) gives a discourse which has
the same introduction and conclusion, and presents in its whole
tenor the most striking similarity with that of Matthew; moreover, in
both cases, Jesus, at the termination of his discourse, goes to
Capernaum, and heals the centurion’s servant. It is true that Luke
gives a later insertion to the discourse, for previous to it he narrates
many journeyings and cures of Jesus, which Matthew places after it;
and while the latter represents Jesus as ascending a mountain, and
being seated there during delivery of his discourse, Luke says,
almost in contradiction to him, that Jesus came down and [335]stood
in the plain. Further, the sermon in Luke contains but a fourth part of
that in Matthew, while it has some elements peculiarly its own.

To avoid the unpleasant admission that one of two inspired

Evangelists must be in error,—which is inevitable if in relation to the
same discourse one of them makes Jesus deliver it on the mountain,
the other in the plain; the one sitting, the other standing; the one
earlier, the other later; if either the one has made important
omissions, or the other as important additions;—the ancient
harmonists pronounced these discourses to be distinct, 2 on the plea
that Jesus must frequently have treated of the essential points of his
doctrine, and may therefore have repeated word for word certain
impressive enunciations. This may be positively denied with respect
to long discourses, and even concise maxims will always be
reproduced in a new guise and connexion by a gifted and inventive
teacher; to say the least, it is impossible that any but a very barren
mind should repeat the same formal exordium, and the same
concluding illustration, on separate occasions.

The identity of the discourses being established, the first effort was
to conciliate or to explain the divergencies between the two
accounts so as to leave their credibility unimpeached. In reference to
the different designation of the locality, Paulus insists on the ἐπὶ of
Luke, which he interprets to imply that Jesus stood over the plain,
and therefore on a hill. Tholuck, more happily, distinguishes the level
space, τόπος πεδινὸς, from the plain properly so called, and regards
it as a less abrupt part of the mountain. But as one Evangelist makes
Jesus ascend the mountain to deliver his discourse, while the other
makes him descend for the same purpose, these conciliators ought
to admit, with Olshausen, that if Jesus taught in the plain, according
to Luke, Matthew has overlooked the descent that preceded the
discourse; or if, as Matthew says, Jesus taught seated on the
mountain, Luke has forgotten to mention that after he had
descended, the pressure of the crowd induced him to reascend
before he commenced his harangue. And without doubt each was
ignorant of what he omits, but each knew that tradition associated
this discourse with a sojourn of Jesus on a mountain. Matthew
thought the mountain a convenient elevation for one addressing a
multitude; Luke, on the contrary, imagined a descent necessary for
the purpose: hence the double discrepancy, for he who teaches from
a mountain is sufficiently elevated over his hearers to sit, but he who
teaches in a plain will naturally stand. The chronological
divergencies, as well as the local, must be admitted, if we would
abstain from fruitless efforts at conciliation. 3

The difference as to the length and contents of the discourse is

susceptible of three explanations: either the concise record of Luke
is a mere extract from the entire discourse which Matthew gives
without abridgment; or Matthew has incorporated many sayings
belonging properly to other occasions; or, lastly, both these causes
of variety have concurred. He who, with Tholuck, wishes to preserve
intact the fides divina, or with Paulus, the fides humana of the
Evangelists, will prefer the first supposition, because to withhold the
true is more innocent than to add the false. The above theologians
hold that the train of thought in the Sermon on the Mount, as given
by Matthew, is closely consecutive, and that this is a proof of its
original unity. But any compiler not totally devoid of ability, can give
a tolerable appearance of connectedness to sayings which did not
originally belong to each other; and even these commentators are
obliged to admit 4 that the alleged consecutiveness [336]extends over
no more than half the sermon, for from vi. 19 it is a string of more
or less isolated sentences, some of them very unlikely to have been
uttered on the occasion. More recent criticism has therefore decided
that the shorter account of Luke presents the discourse of Jesus in
its original form, and that Matthew has taken the licence of
incorporating with this much that was uttered by Jesus at various
times, so as to retain the general sketch—the exordium, peroration,
and essential train of thought; while between these compartments
he inserted many sayings more or less analogous borrowed from
elsewhere. 5 This view is especially supported by the fact that many
of the sentences, which in Matthew make part of the Sermon on the
Mount, are in Mark and Luke dispersed through a variety of scenes.
Compelled to grant this, yet earnestly solicitous to avert from the
Evangelist an imputation that might invalidate his claim to be
considered an eye-witness, other theologians maintain that Matthew
did not compile the discourse under the idea that it was actually
spoken on a single occasion, but with the clearest knowledge that
such was not the case. 6 It is with justice remarked in opposition to
this, that when Matthew represents Jesus as ascending the
mountain before he begins his discourse, and descending after its
close, he obviously makes these two incidents the limits of a single
address; and that when he speaks of the impression which the
discourse produced on the multitude, whose presence he states as
the inducement to its delivery, he could not but intend to convey the
idea of a continuous harangue. 7 As to Luke’s edition of the sermon,
there are parts in which the interrupted connexion betrays
deficiencies, and there are additions which do not look genuine; 8 it is
also doubtful whether he assigns a more appropriate connexion to
the passages in the position of which he differs from Matthew; 9 and
hence, as we shall soon see more fully, he has in this instance no
advantage over his predecessor.

The assemblage to whom the Sermon on the Mount was addressed,

might from Luke’s account be supposed a narrow circle, for he states
that the choice of the apostles immediately preceded the discourse,
and that at its commencement Jesus lifted up his eyes on his
disciples, and he does not, like Matthew, note the multitude, ὄχλους,
as part of the audience. On the other hand, Matthew also mentions
that before the sermon the disciples gathered round Jesus and were
taught by him; and Luke represents the discourse as being delivered
in the audience of the people (vii. 1 ); it is therefore evident that
Jesus spoke to the crowd in general, but with a particular view to
the edification of his disciples. 10 We have no reason to doubt that a
real harangue of Jesus, more than ordinarily solemn and public, was
the foundation of the evangelical accounts before us.

Let us now proceed to an examination of particulars. In both

editions, the Sermon on the Mount is opened by a series of
beatitudes; in Luke, however, not only are several wanting which we
find in Matthew, but most of those common to both are in the
former taken in another sense than in the latter. 11 The poor, πτωχοὶ,
are not specified as in Matthew by the addition, in spirit, τῷ
πνεύματι; they are therefore not those who have a deep
consciousness of inward poverty and misery, but the literally poor;
neither is the [337]hunger of the πεινῶντες (hungering) referred to
τὴν δικαιοσύνην (righteousness); it is therefore not spiritual hunger,
but bodily; moreover, the adverb νῦν, now, definitely marks out
those who hunger and those who weep, the πεινῶντες and
κλαίοντες. Thus in Luke the antithesis is not, as in Matthew, between
the present sorrows of pious souls, whose pure desires are yet
unsatisfied, and their satisfaction about to come; but between
present suffering and future well-being in general. 12 This mode of
contrasting the αἰὼν οὗτος and the αἰὼν μέλλων, the present age
and the future, is elsewhere observable in Luke, especially in the
parable of the rich man; and without here inquiring which of the two
representations is probably the original, I shall merely remark, that
this of Luke is conceived entirely in the spirit of the Ebionites,—a
spirit which has of late been supposed discernible in Matthew. It is a
capital principle with the Ebionites, as they are depicted in the
Clementine Homilies, that he who has his portion in the present age,
will be destitute in the age to come; while he who renounces earthly
possessions, thereby accumulates heavenly treasures. 13 The last
beatitude relates to those who are persecuted for the sake of Jesus.
Luke in the parallel passage has, for the Son of man’s sake; hence
the words for my sake in Matthew, must be understood to refer to
Jesus solely in his character of Messiah. 14

The beatitudes are followed in Luke by as many woes οὐαὶ, which

are wanting in Matthew. In these the opposition established by the
Ebionites between this world and the other, is yet more strongly
marked; for woe is denounced on the rich, the full, and the joyous,
simply as such, and they are threatened with the evils corresponding
to their present advantages, under the new order of things to be
introduced by the Messiah; a view that reminds us of the Epistle of
James, v. 1 ff. The last woe is somewhat stiffly formed after the
model of the last beatitude, for it is evidently for the sake of the
contrast to the true prophets, so much calumniated, that the false
prophets are said, without any historical foundation, to have been
spoken well of by all men. We may therefore conjecture, with
Schleiermacher, 15 that we are indebted for these maledictions to the
inventive fertility of the author of the third gospel. He added this
supplement to the beatitudes, less because, as Schleiermacher
supposes, he perceived a chasm, which he knew not how to fill, than
because he judged it consistent with the character of the Messiah,
that, like Moses of old, he should couple curses with blessings. The
Sermon on the Mount is regarded as the counterpart of the law,
delivered on Mount Sinai; but the introduction, especially in Luke,
reminds us more of a passage in Deuteronomy, in which Moses
commands that on the entrance of the Israelitish people into the
promised land, one half of them shall take their stand on Mount
Gerizim, and pronounce a manifold blessing on the observers of the
law, the other half on Mount Ebal, whence they were to fulminate as
manifold a curse on its transgressors. We read in Josh. viii. 33 ff.
that this injunction was fulfilled. 16
With the beatitudes, Matthew suitably connects the representation of
the [338]disciples as the salt of the earth, and the light of the world
(v. 13 ff. ). In Luke, the discourse on the salt is, with a rather
different opening, introduced in another place (xiv. 34 f .), where
Jesus admonishes his hearers to ponder the sacrifices that must be
made by those who would follow him, and rather to abstain from the
profession of discipleship than to maintain it dishonourably; and to
this succeeds aptly enough the comparison of such degenerate
disciples to salt that has lost its savour. Thus the dictum accords with
either context, and from its aphoristical conciseness would be likely
to recur, so that it may have been really spoken in both discourses.
On the contrary, it cannot have been spoken in the sequence in
which it is placed by Mark (ix. 50 ): for the idea that every one shall
be salted with fire (in allusion to hell), has no internal connexion
with the comparison of the true disciples of Jesus to salt, denoting
their superiority: the connexion is merely external, resulting from the
verbal affinity of ἁλίζειν and ἅλας,—it is the connexion of the
dictionary. 17 The altered sequel which Mark gives to the apothegm
(have salt in yourselves, and be at peace with one another) might
certainly be united to it without incongruity, but it would accord
equally well with quite a different train of thought. The apothegm on
the light which is not to be hidden, as the salt is not to be without
savour, is also wanting in the Sermon on the Mount as given by
Luke; who, however, omitting the special application to the disciples,
has substantially the same doctrine in two different places. We find it
first (viii. 16 ) immediately after the interpretation of the parable of
the sower, where it also occurs in Mark (iv. 21 ), It must be
admitted that there is no incoherence in associating the shining of
the light with the fructification of the seed; still, a judicious teacher
will pause on the interpretation of a parable, and will not disturb its
effect by a hasty transition to new images. At any rate there is no
intrinsic connexion between the shining of the inward light, and the
declaration appended to it by Luke, that all secrets shall be made
manifest. We have here a case which is of frequent recurrence with
this Evangelist; that, namely, of a variety of isolated sayings being
thrown confusedly together between two independent discourses or
narratives. Thus between the parable of the sower and the narrative
of the visit paid to Jesus by his mother and brethren, the apothegm
on the light is inserted on account of its internal analogy with the
parable; then, because in this apothegm there occurs the opposition
between concealment and manifestation, it suggested to the writer
the otherwise heterogeneous discourse on the revelation of all
secrets; whereupon is added, quite irrelevantly to the context, but
with some relation to the parable, the declaration, Whosoever hath,
to him shall be given. In the second passage on the manifestation of
the light (xi. 33 ), the subject has absolutely no connexion, unless
we interpolate one 18 with that of the context, which turns on the
condemnation of the cotemporaries of Jesus by the Ninevites. The
fact is, that here again, between the discourses against the demand
for signs and those at the Pharisee’s dinner, we have a chasm filled
up with disjointed fragments of harangues.

At v. 17 ff . follows the transition to the main subject of the sermon;

the assurance of Jesus that he came not to destroy the law and the
prophets, but to fulfil, etc. Now as Jesus herein plainly presupposes
that he is himself the Messiah, to whom was ascribed authority to
abolish a part of the law, this declaration cannot properly belong to a
period in which, if Matt. xvi. 13 ff . be rightly placed, he had not yet
declared himself to be the Messiah. Luke [339](xvi. 17 ) inserts this
declaration together with the apparently contradictory one, that the
law and the prophets were in force until the coming of John. These
are two propositions that we cannot suppose to have been uttered
consecutively; and the secret of their conjunction in Luke’s gospel
lies in the word νόμος, law, which happens to occur in both. 19 It is to
be observed that between the parable of the steward and that of the
rich man, we have another of those pauses in which Luke is fond of
introducing his fragments.

So little, it appears from v. 20 , is it the design of Jesus to inculcate

a disregard of the Mosaic law, that he requires a far stricter
observance of its precepts than the Scribes and Pharisees, and he
makes the latter appear in contrast to himself as the underminers of
the law. Then follows a series of Mosaic commandments, on which
Jesus comments so as to show that he penetrates into the spirit of
the law, instead of cleaving to the mere letter, and especially
discerns the worthlessness of the rabbinical glosses (48). This
section, in the order and completeness in which we find it in
Matthew, is wanting in Luke’s Sermon on the Mount; a decisive proof
that the latter has deficiencies. For not only does this chapter
contain the fundamental thought of the discourse as given by
Matthew, but the desultory sayings which Luke gives, concerning the
love of enemies, mercifulness and beneficence, only acquire a
definite purpose and point of union in the contrast between the
spiritual interpretation of the law given by Jesus, and the carnal one
given by the doctors of the time. The words, too, with which Luke
makes Jesus proceed after the last woe: But I say unto you, and
those at v. 39 , And he spake a parable unto them, have been
correctly pointed out as indicative of chasms. 20 As regards the
isolated parallel passages, the admonition to a quick reconciliation
with an adversary (v. 25 f. ), is, to say the least, not so easily
brought into connexion with the foregoing matter in Luke (xii. 58 )
as in Matthew. 21 It is still worse with the passage in Luke which is
parallel with Matt. v. 32 ; this text (relative to divorce), which in
Matthew is linked in the general chain of ideas, is in Luke (xvi. 18 )
thrust into one of the apertures we have noticed, between the
assurance of the perpetuity of the law and the parable of the rich
man. Olshausen tries to find a thread of connexion between the
passage and the one preceding it, by interpreting adultery,
μοιχεύειν, allegorically, as faithlessness to the divine law; and
Schleiermacher 22 attaches it to the succeeding parable by referring it
to the adulterous Herod: but such interpretations are altogether
visionary. 23 Probably tradition had apprized the Evangelist that Jesus,
after the foregoing declaration as to the perpetuity of the Mosaic
law, had enunciated his severe principle on the subject of divorce,
and hence he gave it this position, not knowing more of its original
connexion. In Matt. xix. 9 , we find a reiteration of this principle on
an occasion very likely to call it forth. The exhortations to patience
and submissiveness, form, in Matthew, the spiritual interpretation of
the old rule, an eye for an eye, etc., and are therefore a following
out of the previous train of thought. In Luke (vi. 29 ), they are
introduced with much less precision by the command concerning
love to enemies: which command is also decidedly better given in
Matthew as the rectification of the precept, Thou shalt love thy
neighbour, and hate thine enemy (43 ff. ). Again: the observation
that to love friends is nothing more than bad men can do, is, in
Matthew, made, in order to controvert the traditional perversion of
the Mosaic injunction to love one’s neighbour, into a [340]permission
to hate enemies: in Luke, the observation follows the rule,
Whatsoever ye would that men should do to you, etc., which in
Matthew occurs farther on (vii. 12 ) without any connexion. On the
whole, if the passage in Luke from vi. 2–36 , be compared with the
corresponding one in Matthew, there will be found in the latter an
orderly course of thought; in the former, considerable confusion. 24

The warnings against Pharisaic hypocrisy (vi. 1–6 ) are without a

parallel in Luke; but he has one of the model prayer, which recent
criticism has turned not a little to the disadvantage of Matthew. The
ancient harmonists, it is true, had no hesitation in supposing that
Jesus delivered this prayer twice,—in the connexion in which it is
given by Matthew, as well as under the circumstances narrated by
Luke (xi. ff. ). 25 But if Jesus had already in the Sermon on the
Mount given a model prayer, his disciples would scarcely have
requested one afterwards, as if nothing of the kind had occurred;
and it is still more improbable that Jesus would repeat the same
formulary, without any recollection that he had delivered it to these
disciples long before. Hence our most recent critics have decided
that Luke alone has preserved the natural and true occasion on
which this prayer was communicated, and that like many other
fragments, it was interpolated in Matthew’s Sermon on the Mount by
the writer. 26 But the vaunted naturalness of Luke’s representation, I,
for one, cannot discover. Apart from the improbability, admitted even
by the above critics, that the disciples of Jesus should have
remained without any direction to pray until the last journey, in
which Luke places the scene; it is anything but natural that Jesus
should abstain from giving his disciples the exemplar which was in
his mind until they sought for it, and that then he should forthwith
fall into prayer. He had, doubtless, often prayed in their circle from
the commencement of their intercourse; and if so, their request was
superfluous, and must, as in John xiv. 9 , have produced only an
admonition to recollect what they had long seen and heard in his
society. The account of Luke seems to have been framed on mere
conjecture; it was known that the above prayer proceeded from
Jesus, and the further question as to the motive for its
communication, received the gratuitous answer: without doubt his
disciples had asked him for such an exemplar. Without, therefore,
maintaining that Matthew has preserved to us the connexion in
which this prayer was originally uttered by Jesus, we are not the less
in doubt whether it has a more accurate position in Luke. 27 With
regard to the elements of the prayer, it is impossible to deny what
Wetstein says: tota hæc oratio ex formulis Hebræorum concinnata
est; 28 but Fritzsche’s observation is also just, that desires of so
general a nature might be uttered in the prayers of various persons,
even in similar phraseology, without any other cause than the broad
uniformity of human feeling. 29 We may add that the selection and
allocation of the petitions in the prayer are entirely original, and bear
the impress of that religious consciousness which Jesus possessed
and sought to impart to his followers. 30 Matthew inserts after the
conclusion of the prayer two propositions, which are properly the
corollary of the third petition, but which seem inaptly placed, not
only because they are severed by the concluding petition from the
passage to which they have reference, but because they have no
point of coincidence [341]with the succeeding censures and
admonitions which turn on the hypocrisy of the Pharisaic fasts. Mark,
however, has still more infelicitously appended these propositions to
the discourse of Jesus on the efficacy of believing prayer (xi. 25 ). 31

At vi. 19 , the thread of strict connexion is broken, according to the

admission of Paulus, and so far all expositors are bound to agree
with him. But his position, that notwithstanding the admitted lack of
coherence in the succeeding collection of sentences, Jesus spoke
them consecutively, is not equally tenable; on the contrary, our more
recent critics have all the probabilities on their side when they
suppose, that in this latter half of the Sermon on the Mount Matthew
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